Tissue sparing, behavioral recovery, supraspinal axonal sparing/regeneration following sub-acute glial transplantation in a model of spinal cord contusion

BMC Neuroscience

Volumn 14, Issue , 2013, Pages

  Barbour, Helen R ^b   Plant, Christine D ^a   Harvey, Alan R ^b   Plant, Giles W ^a,b  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Behavioral recovery; Glia; Spinal cord injury; Tissue sparing; Transplantation

Indexed keywords

CHONDROITIN; FLUOROGOLD; PROTEOGLYCAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL NUCLEUS; CELL TRANSPLANTATION; CONTROLLED STUDY; CONTUSION; FEMALE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LOCOMOTION; NERVE FIBER REGENERATION; NONHUMAN; OLFACTORY ENSHEATHING CELL; OPEN FIELD BEHAVIOR; OPEN FIELD TEST; PROTEOGLYCAN SYNTHESIS; RAPHE NUCLEUS; RAT; SCHWANN CELL; SPINAL CORD; SPINAL CORD CONTUSION; SPINAL CORD INJURY; STAINING; SUBACUTE GLIAL TRANSPLANTATION; TREATMENT OUTCOME; VESTIBULAR SYSTEM; WALKING;

ANIMALS; AXONS; DISEASE MODELS, ANIMAL; FEMALE; IMMUNOHISTOCHEMISTRY; NERVE REGENERATION; NEUROGLIA; RATS; RATS, INBRED F344; RECOVERY OF FUNCTION; SPINAL CORD INJURIES;

EID: 84884606253     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-14-106     Document Type: Article

References (109)

1. Doucette R. PNS-CNS transitional zone of the first cranial nerve. J Comp Neurol 1991, 312(3):451-466. 10.1002/cne.903120311, 1748741.
2. Ramer LM, Richter MW, Roskams AJ, Tetzlaff W, Ramer MS. Peripherally-derived olfactory ensheathing cells do not promote primary afferent regeneration following dorsal root injury. Glia 2004, 47(2):189-206. 10.1002/glia.20054, 15185397.
3. Richter MW, Roskams AJ. Olfactory ensheathing cell transplantation following spinal cord injury: Hype or hope?. Exp Neurol 2008, 209(2):353-367. 10.1016/j.expneurol.2007.06.011, 17643431.
4. Ruitenberg MJ, Vukovic J, Sarich J, Busfield SJ, Plant GW. Olfactory ensheathing cells: characteristics genetic engineering and therapeutic potential. J Neurotrauma 2006, 23(3-4):468-478.
5. Graziadei PP, Monti Graziadei GA. Neurogenesis and neuron regeneration in the olfactory system of mammals III. Deafferentation and reinnervation of the olfactory bulb following section of the fila olfactoria in rat. J Neurocytol 1980, 9(2):145-162. 10.1007/BF01205155, 7441292.
6. Monti Graziadei GA, Karlan MS, Bernstein JJ, Graziadei PP. Reinnervation of the olfactory bulb after section of the olfactory nerve in monkey (Saimiri sciureus). Brain Res 1980, 189(2):343-354. 10.1016/0006-8993(80)90095-5, 6768424.
7. Li Y, Field PM, Raisman G. Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 1997, 277(5334):2000-2002. 10.1126/science.277.5334.2000, 9302296.
8. Plant GW, Christensen CL, Oudega M, Bunge MB. Delayed transplantation of olfactory ensheathing glia promotes sparing/regeneration of supraspinal axons in the contused adult rat spinal cord. J Neurotrauma 2003, 20(1):1-16. 10.1089/08977150360517146, 12614584.
9. Ramon-Cueto A, Plant GW, Avila J, Bunge MB. Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J Neurosci 1998, 18(10):3803-3815.
10. Ramon-Cueto A, Cordero MI, Santos-Benito FF, Avila J. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 2000, 25(2):425-435. 10.1016/S0896-6273(00)80905-8, 10719896.
11. Ruitenberg MJ, Levison DB, Lee SV, Verhaagen J, Harvey AR, Plant GW. NT-3 expression from engineered olfactory ensheathing glia promotes spinal sparing and regeneration. Brain 2005, 128(Pt 4):839-853.
12. Ruitenberg MJ, Plant GW, Christensen CL, Blits B, Niclou SP, Harvey AR, Boer GJ, Verhaagen J. Viral vector-mediated gene expression in olfactory ensheathing glia implants in the lesioned rat spinal cord. Gene Ther 2002, 9(2):135-146. 10.1038/sj.gt.3301626, 11857072.
13. Ruitenberg MJ, Plant GW, Hamers FP, Wortel J, Blits B, Dijkhuizen PA, Gispen WH, Boer GJ, Verhaagen J. Ex vivo adenoviral vector-mediated neurotrophin gene transfer to olfactory ensheathing glia: effects on rubrospinal tract regeneration lesion size and functional recovery after implantation in the injured rat spinal cord. J Neurosci 2003, 23(18):7045-7058.
14. Takami T, Oudega M, Bates ML, Wood PM, Kleitman N, Bunge MB. Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J Neurosci 2002, 22(15):6670-6681.
15. Guest JD, Rao A, Olson L, Bunge MB, Bunge RP. The ability of human Schwann cell grafts to promote regeneration in the transected nude rat spinal cord. Exp Neurol 1997, 148(2):502-522. 10.1006/exnr.1997.6693, 9417829.
16. Imaizumi T, Lankford KL, Burton WV, Fodor WL, Kocsis JD. Xenotransplantation of transgenic pig olfactory ensheathing cells promotes axonal regeneration in rat spinal cord. Nature Biotech 2000, 18(9):949-953.
17. Xu XM, Chen A, Guenard V, Kleitman N, Bunge MB. Bridging Schwann cell transplants promote axonal regeneration from both the rostral and caudal stumps of transected adult rat spinal cord. J Neurocytol 1997, 26(1):1-16. 10.1023/A:1018557923309, 9154524.
18. Xu XM, Guenard V, Kleitman N, Bunge MB. Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J Comp Neurol 1995, 351(1):145-160. 10.1002/cne.903510113, 7896937.
19. Morrissey TK, Kleitman N, Bunge RP. Isolation and functional characterization of Schwann cells derived from adult peripheral nerve. J Neurosci 1991, 11(8):2433-2442.
20. Pearse DD, Barakat DJ. Cellular repair strategies for spinal cord injury. Expert Op Biol Ther 2006, 6(7):639-652.
21. Pearse DD, Sanchez AR, Pereira FC, Andrade CM, Puzis R, Pressman Y, Golden K, Kitay BM, Blits B, Wood PM, Bunge MB. Transplantation of Schwann cells and/or olfactory ensheathing glia into the contused spinal cord: Survival migration axon association and functional recovery. Glia 2007, 55(9):976-1000. 10.1002/glia.20490, 17526000.
22. Plant GW Ramon-Cueto A, Bunge MB. Transplantation of Schwann cell of Schwann cells and ensheathing glia to improve regeneration in adult spinal cord. Axonal Regeneration in the Central Nervous System 2001a, 529-561. New York and Basel: Marcel Dekker Inc, Ingoglia N, Murray M.
23. Harvey AR, Plant GW. Olfactory ensheathing glia and spinal cord injury: basic mechanisms to transplantation. Fut Neurol 2006, 1(4):453-463.
24. van den Pol AN, Santarelli JG. Olfactory ensheathing cells: time lapse imaging of cellular interactions axonal support rapid morphologic shifts and mitosis. J Comp Neurol 2003, 458(2):175-194. 10.1002/cne.10577, 12596257.
25. Vincent AJ, West AK, Chuah MI. Morphological plasticity of olfactory ensheathing cells is regulated by cAMP and endothelin-1. Glia 2003, 41(4):393-403. 10.1002/glia.10171, 12555206.
26. Vukovic J, Ruitenberg MJ, Roet K, Franssen E, Arulpragasam A, Sasaki T, Verhaagen J, Harvey AR, Busfield SJ, Plant GW. The glycoprotein fibulin-3 regulates morphology and motility of olfactory ensheathing cells in vitro. Glia 2009, 57(4):424-443. 10.1002/glia.20771, 18803302.
27. Ramon-Cueto A, Perez J, Nieto-Sampedro M. In vitro enfolding of olfactory neurites by p75 NGF receptor positive ensheathing cells from adult rat olfactory bulb. Eur J Neurosci 1993, 5(9):1172-1180. 10.1111/j.1460-9568.1993.tb00971.x, 8281321.
28. Lu J, Feron F, Ho SM, Mackay-Sim A, Waite PM. Transplantation of nasal olfactory tissue promotes partial recovery in paraplegic adult rats. Brain Res 2001, 889(1-2):344-357.
29. Lu P, Yang H, Culbertson M, Graham L, Roskams J, Tuszynski MH. Olfactory Ensheathing Cells Do Not Exhibit Unique Migratory or Axonal Growth-Promoting Properties after Spinal Cord Injury. J Neurosci 2006, 26:11120-11130. 10.1523/JNEUROSCI.3264-06.2006, 17065452.
30. Richter MW, Fletcher PA, Liu J, Tetzlaff W, Roskams AJ. Lamina propria and olfactory bulb ensheathing cells exhibit differential integration and migration and promote differential axon sprouting in the lesioned spinal cord. J Neurosci 2005, 25(46):10700-10711. 10.1523/JNEUROSCI.3632-05.2005, 16291943.
31. Boyd JG, Lee J, Skihar V, Doucette R, Kawaja MD. LacZ-expressing olfactory ensheathing cells do not associate with myelinated axons after implantation into the compressed spinal cord. Proc Natl Acad Sci U S A 2004, 101(7):2162-2166. 10.1073/pnas.0303842101, 357069, 14764892.
32. Nagoshi N, Shibata S, Hamanoue M, Mabuchi Y, Matsuzaki Y, Toyama Y, Nakamura M, Okano H. Schwann cell plasticity after spinal cord injury shown by neural crest lineage tracing. Glia 2011, 59(5):771-784. 10.1002/glia.21150, 21351159.
33. Plant GW, Currier PF, Cuervo EP, Bates ML, Pressman Y, Bunge MB, Wood PM. Purified adult ensheathing glia fail to myelinate axons under culture conditions that enable Schwann cells to form myelin. J Neurosci 2002, 22(14):6083-6091.
34. DiStefano PS, Johnson EM. Identification of a truncated form of the nerve growth factor receptor. Proc Natl Acad Sci U S A 1988, 85(1):270-274. 10.1073/pnas.85.1.270, 279526, 2829174.
35. Zupan AA, Johnson EM. Evidence for endocytosis-dependent proteolysis in the generation of soluble truncated nerve growth factor receptors by A875 human melanoma cells. J Biol Chem 1991, 266(23):15384-15390.
36. Hu Y, Leaver SG, Plant GW, Hendriks WT, Niclou SP, Verhaagen J, Harvey AR, Cui Q. Lentiviral-mediated transfer of CNTF to schwann cells within reconstructed peripheral nerve grafts enhances adult retinal ganglion cell survival and axonal regeneration. Mol Ther 2005, 11(6):906-915. 10.1016/j.ymthe.2005.01.016, 15922961.
37. Leaver SG, Harvey AR, Plant GW. Adult olfactory ensheathing glia promote the long-distance growth of adult retinal ganglion cell neurites in vitro. Glia 2006, 53(5):467-476. 10.1002/glia.20311, 16355371.
38. Schwartz M, Yoles E. Immune-based therapy for spinal cord repair: autologous macrophages and beyond. J Neurotrauma 2006, 23(3-4):360-370.
39. Cummings BJ, Uchida N, Tamaki SJ, Salazar DL, Hooshmand M, Summers R, Gage FH, Anderson AJ. Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc Natl Acad Sci U S A 2005, 102(39):14069-14074. 10.1073/pnas.0507063102, 1216836, 16172374.
40. Iwanami A, Kaneko S, Nakamura M, Kanemura Y, Mori H, Kobayashi S, Yamasaki M, Momoshima S, Ishii H, Ando K, Tanioka Y, Tamaoki N, Nomura T, Toyama Y, Okano H. Transplantation of human neural stem cells for spinal cord injury in primates. J Neurosci Res 2005, 80(2):182-190. 10.1002/jnr.20436, 15772979.
41. Koshizuka S, Okada S, Okawa A, Koda M, Murasawa M, Hashimoto M, Kamada T, Yoshinaga K, Murakami M, Moriya H, Yamazaki M. Transplanted hematopoietic stem cells from bone marrow differentiate into neural lineage cells and promote functional recovery after spinal cord injury in mice. J Neuropath and Exp Neurol 2004, 63(1):64-72.
42. Barakat DJ, Gaglani SM, Neravetla SR, Sanchez AR, Andrade CM, Pressman Y, Puzis R, Garg MS, Bunge MB, Pearse DD. Survival, integration, and axon growth support of glia transplanted into the chronically contused spinal cord. Cell Transplant 2005, 14(4):225-240. 10.3727/000000005783983106, 15929557.
43. Sasaki M, Lankford KL, Zemedkun M, Kocsis JD. Identified olfactory ensheathing cells transplanted into the transected dorsal funiculus bridge the lesion and form myelin. J Neurosci 2004, 24(39):8485-8493. 10.1523/JNEUROSCI.1998-04.2004, 2605369, 15456822.
44. Hill CE, Moon LD, Wood PM, Bunge MB. Labeled Schwann cell transplantation: cell loss, host Schwann cell replacement, and strategies to enhance survival. Glia 2006, 53(3):338-343. 10.1002/glia.20287, 16267833.
45. Beattie MS, Bresnahan JC, Komon J, Tovar CA, Van Meter M, Anderson DK, Faden AI, Hsu CY, Noble LJ, Salzman S, Young W. Endogenous repair after spinal cord contusion injuries in the rat. Exp Neurol 1997, 148(2):453-463. 10.1006/exnr.1997.6695, 9417825.
46. Boruch AV, Conners JJ, Pipitone M, Deadwyler G, Storer PD, Devries GH, Jones KJ. Neurotrophic and migratory properties of an olfactory ensheathing cell line. Glia 2001, 33(3):225-229. 10.1002/1098-1136(200103)33:3<225::AID-GLIA1021>3.0.CO;2-Y, 11241740.
47. Cao L, Liu L, Chen ZY, Wang LM, Ye JL, Qiu HY, Lu CL, He C. Olfactory ensheathing cells genetically modified to secrete GDNF to promote spinal cord repair. Brain 2004, 127(3):535-549.
48. Woodhall E, West AK, Chuah MI. Cultured olfactory ensheathing cells express nerve growth factor brain-derived neurotrophic factor glia cell line-derived neurotrophic factor and their receptors. Brain Res Mol Brain Res 2001, 88(1-2):203-213.
49. Fairless R, Frame MC, Barnett SC. N-cadherin differentially determines Schwann cell and olfactory ensheathing cell adhesion and migration responses upon contact with astrocytes. Mol Cell Neurosci 2005, 28(2):253-263. 10.1016/j.mcn.2004.09.009, 15691707.
50. Grimpe B, Dong S, Doller C, Temple K, Malouf AT, Silver J. The critical role of basement membrane-independent laminin gamma 1 chain during axon regeneration in the CNS. J Neurosci 2002, 22(8):3144-3160.
51. Tom VJ, Doller CM, Malouf AT, Silver J. Astrocyte-associated fibronectin is critical for axonal regeneration in adult white matter. J Neurosci 2004, 24(42):9282-9290. 10.1523/JNEUROSCI.2120-04.2004, 15496664.
52. Horky LL, Galimi F, Gage FH, Horner PJ. Fate of endogenous stem/progenitor cells following spinal cord injury. J Comp Neurol 2006, 498(4):525-538. 10.1002/cne.21065, 2553041, 16874803.
53. Lee IH, Bulte JW, Schweinhardt P, Douglas T, Trifunovski A, Hofstetter C, Olson L, Spenger C. In vivo magnetic resonance tracking of olfactory ensheathing glia grafted into the rat spinal cord. Exp Neurol 2004, 187(2):509-516. 10.1016/j.expneurol.2004.02.007, 15144877.
54. Ramon-Cueto A, Nieto-Sampedro M. Regeneration into the spinal cord of transected dorsal root axons is promoted by ensheathing glia transplants. Exp Neurol 1994, 127(2):232-244. 10.1006/exnr.1994.1099, 8033963.
55. Duncan ID, Aguayo AJ, Bunge RP, Wood PM. Transplantation of rat Schwann cells grown in tissue culture into the mouse spinal cord. J Neurol Sci 1981, 49(2):241-252. 10.1016/0022-510X(81)90082-4, 7217983.
56. Symons NA, Danielsen N, Harvey AR. Migration of cells into and out of peripheral nerve isografts in the peripheral and central nervous systems of the adult mouse. Eur J Neurosci 2001, 14(3):522-532. 10.1046/j.0953-816x.2001.01681.x, 11553302.
57. Plant GW, Bates ML, Bunge MB. Inhibitory proteoglycan immunoreactivity is higher at the caudal than the rostral Schwann cell graft-transected spinal cord interface. Mol Cell Neurosci 2001, 17(3):471-487. 10.1006/mcne.2000.0948, 11273643.
58. Doucette R. Glial cells in the nerve fiber layer of the main olfactory bulb of embryonic and adult mammals. Microsc Res Tech 1993, 24(2):113-130. 10.1002/jemt.1070240204, 8457724.
59. Lemke G. Glial control of neuronal development. Ann Rev Neurosci 2001, 24:87-105. 10.1146/annurev.neuro.24.1.87, 11283306.
60. Ruitenberg MJ, Vukovic J, Blomster L, Hall JM, Jung S, Filgueira L, McMenamin PG, Plant GW. CX3CL1/fractalkine regulates branching and migration of monocyte-derived cells in the mouse olfactory epithelium. J Neuroimmunol 2008, 205(1-2):80-85.
61. Chinnery HR, Ruitenberg MJ, Plant GW, Pearlman E, Jung S, McMenamin PG. The chemokine receptor CX3CR1 mediates homing of MHC class II-positive cells to the normal mouse corneal epithelium. Invest Ophthalmol Vis Sci 2007, 48(4):1568-1574. 10.1167/iovs.06-0746, 3392181, 17389486.
62. Roet KC, Bossers K, Franssen EH, Ruitenberg MJ, Verhaagen J. A meta-analysis of microarray-based gene expression studies of olfactory bulb-derived olfactory ensheathing cells. Exp Neurol 2011, 229(1):10-45. 10.1016/j.expneurol.2011.03.001, 21396936.
63. Shihabuddin LS, Ray J, Gage FH. FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Exp Neurol 1997, 148(2):577-586. 10.1006/exnr.1997.6697, 9417834.
64. McTigue DM, Horner PJ, Stokes BT, Gage FH. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J Neurosci 1998, 18(14):5354-5365.
65. Horner PJ, Power AE, Kempermann G, Kuhn HG, Palmer TD, Winkler J, Thal LJ, Gage FH. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 2000, 20(6):2218-2228.
66. Lytle JM, Wrathall JR. Glial cell loss proliferation and replacement in the contused murine spinal cord. Eur J Neurosci 2007, 25(6):1711-1724. 10.1111/j.1460-9568.2007.05390.x, 17432960.
67. Yang H, Lu P, McKay HM, Bernot T, Keirstead H, Steward O, Gage FH, Edgerton VR, Tuszynski MH. Endogenous neurogenesis replaces oligodendrocytes and astrocytes after primate spinal cord injury. J Neurosci 2006, 26(8):2157-2166. 10.1523/JNEUROSCI.4070-05.2005, 16495442.
68. Adrian EK. Cell division in injured spinal cord. Am J Anat 1968, 123(3):501-520. 10.1002/aja.1001230307, 5727100.
69. Adrian EK, Williams MG, George FC. Fine structure of reactive cells in injured nervous tissue labeled with 3H-thymidine injected before injury. J Comp Neurol 1978, 180(4):815-839. 10.1002/cne.901800412, 681551.
70. Kojima A, Tator CH. Intrathecal administration of epidermal growth factor and fibroblast growth factor 2 promotes ependymal proliferation and functional recovery after spinal cord injury in adult rats. J Neurotrauma 2002, 19(2):223-238. 10.1089/08977150252806974, 11893024.
71. Santos-Silva A, Fairless R, Frame MC, Montague P, Smith GM, Toft A, Riddell JS, Barnett SC. FGF/heparin differentially regulates Schwann cell and olfactory ensheathing cell interactions with astrocytes: a role in astrocytosis. J Neurosci 2007, 27(27):7154-7167. 10.1523/JNEUROSCI.1184-07.2007, 17611269.
72. Goritz C, Dias DO, Tomilin N, Barbacid M, Shupliakov O, Frisen J. A pericyte origin of spinal cord scar tissue. Science 2011, 333(6039):238-242. 10.1126/science.1203165, 21737741.
73. Decimo I, Bifari F, Rodriguez FJ, Malpeli G, Dolci S, Lavarini V, Pretto S, Vasquez S, Sciancalepore M, Montalbano A, Berton V, Krampera M, Fumagalli G. Nestin- and doublecortin-positive cells reside in adult spinal cord meninges and participate in injury-induced parenchymal reaction. Stem Cells 2011, 29(12):2062-2076. 10.1002/stem.766, 3468739, 22038821.
74. Barnabe-Heider F, Gorit C, Sabelstrom H, Takebayashi H, Pfrieger FW, Meletis K, Frisen J. Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 2010, 7(4):470-482. 10.1016/j.stem.2010.07.014, 20887953.
75. Meletis K, Barnabe-Heider F, Carlen M, Evergren E, Tomilin N, Shupliakov O, Frisen J. Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol 2008, 6(7):e182. 10.1371/journal.pbio.0060182, 2475541, 18651793.
76. Casella GT, Marcillo A, Bunge MB, Wood PM. New vascular tissue rapidly replaces neural parenchyma and vessels destroyed by a contusion injury to the rat spinal cord. Exp Neurol 2002, 173(1):63-76. 10.1006/exnr.2001.7827, 11771939.
77. Brook GA, Plate D, Franzen R, Martin D, Moonen G, Schoenen J, Schmitt AB, Noth J, Nacimiento W. Spontaneous longitudinally orientated axonal regeneration is associated with the Schwann cell framework within the lesion site following spinal cord compression injury of the rat. J Neurosci Res 1998, 53(1):51-65. 10.1002/(SICI)1097-4547(19980701)53:1<51::AID-JNR6>3.0.CO;2-I, 9670992.
78. Hill CE, Beattie MS, Bresnahan JC. Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp Neurol 2001, 171(1):153-169. 10.1006/exnr.2001.7734, 11520130.
79. O'Brien DF, Farrell M, Fraher JP, Bolger C. Schwann cell invasion of the conus medullaris: case report. Eur Spine J 2003, 12(3):328-331. 3615487, 12800008.
80. Lakatos A, Barnett SC, Franklin RJ. Olfactory ensheathing cells induce less host astrocyte response and chondroitin sulphate proteoglycan expression than Schwann cells following transplantation into adult CNS white matter. Exp Neurol 2003, 184(1):237-246. 10.1016/S0014-4886(03)00270-X, 14637095.
81. Ramon-Cueto A, Avila J. Olfactory ensheathing glia: properties and function. Brain Res Bull 1998, 46(3):175-187. 10.1016/S0361-9230(97)00463-2, 9667810.
82. Gueye Y, Ferhat L, Sbai O, Bianco J, Ould-Yahoui A, Bernard A, Charrat E, Chauvin JP, Risso JJ, Feron F, Rivera S, Khrestchatisky M. Trafficking and secretion of matrix metalloproteinase-2 in olfactory ensheathing glial cells: A role in cell migration?. Glia 2011, 59(5):750-770. 10.1002/glia.21146, 21360755.
83. Li Y, Li D, Raisman G. Interaction of olfactory ensheathing cells with astrocytes may be the key to repair of tract injuries in the spinal cord: the 'pathway hypothesis'. J Neurocytol 2005, 34(3-5):343-351.
84. Tisay KT, Key B. The extracellular matrix modulates olfactory neurite outgrowth on ensheathing cells. J Neurosci 1999, 19(22):9890-9899.
85. Franssen EH, Roet KC, de Bree FM, Verhaagen J. Olfactory ensheathing glia and Schwann cells exhibit a distinct interaction behavior with meningeal cells. J Neurosci Res 2009, 87:1556-1564. 10.1002/jnr.21979, 19140223.
86. Obremski VJ, Johnson MI, Bunge MB. Fibroblasts are required for Schwann cell basal lamina deposition and ensheathment of unmyelinated sympathetic neurites in culture. J Neurocytol 1993, 22(2):102-117. 10.1007/BF01181574, 8445407.
87. Ibanez C, Ito D, Zawadzka M, Jeffery ND, Franklin RJ. Calponin is expressed by fibroblasts and meningeal cells but not olfactory ensheathing cells in the adult peripheral olfactory system. Glia 2007, 55(2):144-151. 10.1002/glia.20443, 17078028.
88. Barnett SC, Alexander CL, Iwashita Y, Gilson JM, Crowther J, Clark L, Dunn LT, Papanastassiou V, Kennedy PG, Franklin RJ. Identification of a human olfactory ensheathing cell that can effect transplant-mediated remyelination of demyelinated CNS axons. Brain 2000, 123(8):1581-1588. 10.1093/brain/123.8.1581, 10908188.
89. Boyd JG, Jahed A, McDonald TG, Krol KM, Van Eyk JE, Doucette R, Kawaja MD. Proteomic evaluation reveals that olfactory ensheathing cells but not Schwann cells express calponin. Glia 2006, 53(4):434-440. 10.1002/glia.20299, 16345031.
90. Li Y, Field PM, Raisman G. Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J Neurosci 1998, 18(24):10514-10524.
91. Lakatos A, Franklin RJ, Barnett SC. Olfactory ensheathing cells and Schwann cells differ in their in vitro interactions with astrocytes. Glia 2000, 32(3):214-225. 10.1002/1098-1136(200012)32:3<214::AID-GLIA20>3.0.CO;2-7, 11102963.
92. Trang T, Beggs S, Wan X, Salter MW. P2X4-receptor-mediated synthesis and release of brain-derived neurotrophic factor in microglia is dependent on calcium and p38-mitogen-activated protein kinase activation. J Neurosci 2009, 29(11):3518-3528. 10.1523/JNEUROSCI.5714-08.2009, 3589565, 19295157.
93. Heumann R, Lindholm D, Bandtlow C, Meyer M, Radeke M, Misko TP J, Shooter E, Thoenen H. Differential regulation of mRNA encoding nerve growth factor and its receptor in rat sciatic nerve during development, degeneration, and regeneration: role of macrophages. Proc Natl Acad Sci U S A 1987, 84(23):8735-8739. 10.1073/pnas.84.23.8735, 299621, 2825206.
94. Meier C, Parmantier E, Brennan A, Mirsky R, Jessen KR. Developing Schwann cells acquire the ability to survive without axons by establishing an autocrine circuit involving insulin-like growth factor neurotrophin-3 and platelet-derived growth factor-BB. J Neurosci 1999, 19(10):3847-3859.
95. Dowsing BJ, Morrison WA, Nicola NA, Starkey GP, Bucci T, Kilpatrick TJ. Leukemia inhibitory factor is an autocrine survival factor for Schwann cells. J Neurochem 1999, 73(1):96-104.
96. Edgerton VR, Roy RR. Paralysis recovery in humans and model systems. Curr Opin Neurobiol 2002, 12(6):658-667. 10.1016/S0959-4388(02)00379-3, 12490256.
97. Kubasak MD, Jindrich DL, Zhong H, Takeoka A, McFarland KC, Munoz-Quiles C, Roy RR, Edgerton VR, Ramon-Cueto A, Phelps PE. OEG implantation and step training enhance hindlimb-stepping ability in adult spinal transected rats. Brain 2008, 131(Pt 1):264-276. 2916741, 18056162.
98. Takeoka A, Kubasak MD, Zhong H, Roy RR, Phelps PE. Serotonergic innervation of the caudal spinal stump in rats after complete spinal transection: effect of olfactory ensheathing glia. J Comp Neurol 2009, 515(6):664-676. 10.1002/cne.22080, 2828942, 19496067.
99. Basso DM, Beattie MS, Bresnahan JC. Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp Neurol 1996, 139(2):244-256. 10.1006/exnr.1996.0098, 8654527.
100. Fitch MT, Doller C, Combs CK, Landreth GE, Silver J. Cellular and molecular mechanisms of glial scarring and progressive cavitation: in vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. J Neurosci 1999, 19(19):8182-8198.
101. McKeon RJ, Schreiber RC, Rudge JS, Silver J. Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 1991, 11(11):3398-3411.
102. Alilain WJ, Horn KP, Hu H, Dick TE, Silver J. Functional regeneration of respiratory pathways after spinal cord injury. Nature 2011, 475(7355):196-200. 10.1038/nature10199, 3163458, 21753849.
103. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002, 416(6881):636-640. 10.1038/416636a, 11948352.
104. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L, Trono D. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 1998, 72(12):9873-9880. 110499, 9811723.
105. Gruner JA. A monitored contusion model of spinal cord injury in the rat. J Neurotrauma 1992, 9(2):123-126. discussion 126-128, 10.1089/neu.1992.9.123, 1404425.
106. Metz GA, Whishaw IQ. Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore- and hindlimb stepping placing and co-ordination. J Neurosci Meths 2002, 115(2):169-179.
107. Bates KA, Fonte J, Robertson TA, Martins RN, Harvey AR. Chronic gliosis triggers Alzheimer's disease-like processing of amyloid precursor protein. Neuroscience 2002, 113(4):785-796. 10.1016/S0306-4522(02)00230-0, 12182886.
108. Oudega M, Vargas CG, Weber AB, Kleitman N, Bunge MB. Long-term effects of methylprednisolone following transection of adult rat spinal cord. Eur J Neurosci 1999, 11(7):2453-2464. 10.1046/j.1460-9568.1999.00666.x, 10383635.
109. West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991, 231(4):482-497. 10.1002/ar.1092310411, 1793176.